The "principle of microbial infallibility" (Alexander, Advances in Applied Microbiology 7: 35-80 (1965)) is an expression of the empirical observation that there are no natural organic compounds which are totally resistant to biodegradation provided favorable environmental conditions. The postulate is that biopolymers have evolved over billions of years and parallel evolution of microbes which derive energy from the catabolism of such molecules has kept pace.
However, the last half century has ushered in the explosive development of synthetic organic chemistry which has yielded the large-scale production of a staggering array of synthetic organic compounds. Many of these compounds have been released, either intentionally or by accident, into the environment.
Many synthetic organic compounds are sufficiently similar to natural compounds to be recognized and degraded by microbes. However, there is another class of synthetic organics which possess molecular structures and chemical bond sequences which are not recognized by microbial enzymes. These compounds, as a class, are referred to as xenobiotics. Xenobiotic compounds are either totally resistant to degradation (recalcitrant), or are-metabolized incompletely. Common features of recalcitrant compounds include, for example, unusual substitutions such as chlorine and other halogens, unusual bonds or bond sequences such as tertiary and quaternary carbon atoms, highly condensed aromatic rings, excessive molecular size, etc.
A xenobiotic class which has proven to be particularly damaging to the environment is the polychlorinated biphenyl (PCB) class. These compounds consist of a biphenyl ring structure with varying degrees of chlorine substitution. PCBs exhibit an array of interesting and useful traits which are generally dependent upon their degree of chlorination. Prior to the ban on PCB production in the United States, the compounds were commonly used as insulators, flame retardants and lubricants. Through widespread use, PCBs became essentially ubiquitous in the environment, concentrating primarily in soils and sediments due to their insolubility in water and bioconcentration in the fatty tissue of many animal species. Recognition of their deleterious effects on fragile ecosystems and human health has led to the investigation of methods for the remediation of contaminated matrices. To date, however, the method of choice remains dredging of sediments and soils, followed by incineration, a generally inefficient process resulting in the liberation of dioxins and furans.
Alternative methods have been sought, but thus far, none have proven both efficient and cost effective. In light of the presence of a biphenyl nucleus which may be attacked by a number of organisms, PCBs would appear to be prime candidates for biodegradation. This, however, has not proven to be the case. PCBs have been found to be extremely resistant to biodegradation, a circumstance which has contributed to their longevity in the environment. Among the reasons for this recalcitrance is the high degree of variability in size and charge between individual molecules of a given PCB. Unlike most compounds, PCBs as manufactured are mixtures varying in the number and position of chlorine atoms attached to the biphenyl core, with the average weight % of chlorine serving as the common basis for classifying these substances. Thus, biodegradation of these mixtures would require that the organisms involved possess enzyme systems with an unusually low substrate specificity. Further, the transformation products themselves are toxic to the organisms which produce them. Most notable of these by-products are two compounds which are generated after cleavage of the biphenyl core. These are chlorobenzoates and chlorocatechols. These compounds inhibit dioxygenase, which in turn catalyzes the initial hydroxylation of PCBs. Although both of these groups of compounds have the potential for biodegradation, organisms which exhibit the capacity to do so are notably lacking in PCB contaminated soils.
It may be speculated that it is these two blocks to mineralization, enzyme specificity and generation of toxic transformation products, which lead to two patterns of weathering found in PCB contaminated soils and sediments. One is the utilization of low molecular weight species leading to the apparent accumulation of the high molecular weight congeners. The other opposing possibility is the degradation of all cogeners, with the progressive dechlorination of high molecular weight species leading to an apparent accumulation of lower weight forms. Both of these are self limiting, either as the system runs out of cogeners, which fit the available battery of enzymes, or as toxic intermediate accumulate, opening the feedback "switch."
This situation, in which the genetic material to carry out the entire process is available in separate organisms, would appear to be ideally suited to the talents of the biotechnology industry which, through cloning techniques, could theoretically combine these traits in a single cell. However, the release of manipulated organisms into the environment on a large scale is strictly regulated, negating the potential utility of such an approach.